Eur J Plant Pathol
https://doi.org/10.1007/s10658-019-01900-1
Host weed species range of Meloidogyne ethiopica
whitehead (Tylenchida: Meloidogynidae) found in Brazil
Cristiano Bellé & Rodrigo Ferraz Ramos &
Ricardo Rubin Balardin & Daiane Dalla Nora
Tiago Edu Kaspary
Accepted: 18 November 2019
# Koninklijke Nederlandse Planteziektenkundige Vereniging 2019
Abstract Meloidogyne ethiopica is considered to be
one of the most economically important emerging nem-
atode species, reported to cause crop losses to several
hosts worldwide. The significance of this species is due
to its high virulence and degree of polyphagia, in addi-
tion to persisting on weed hosts within agricultural
fields. This study evaluated the host status of 36 differ-
ent weed species, confirming the polyphagia habit of
M. ethiopica and indicating which plant species may be
alternative hosts for this plant nematode. Weed species
were inoculated with 5000 eggs and second-stage juve-
niles (J2) of M. ethiopica, with gall index (GI),
nematode/g root (Nem/g), and reproduction factor
(RF) value determined following 60 days post inocula-
tion. The data obtained indicate that many weed species
may be excellent hosts for M. ethiopica. Plants deemed
susceptible (RF ≥ 1.0) were: Acanthospermum australe,
Amaranthus deflexus, A. hybridus, A. spinosus,
A . v i r i d i s , Bi de n s p i l o s a, B. su ba lt er na n s,
C a rd i o s p e r m u m h a l i c a c a b u m , C o m m e l i n a
benghalensis, Cynodon dactylon, Euphorbia
heterophylla, Galinsoga parviflora, Ipomoea
grandifolia, I. nil, I. purpurea, Leonurus sibiricus,
Nicandra physaloides, Oxalis corniculata, Portulaca
C. Bellé (*) : R. F. Ramos : R. R. Balardin
Universidade Federal de Santa Maria, Centro de Ciências Rurais,
Santa Maria, Rio Grande do Sul, Brazil
e-mail: crbelle@gmail.com
T. E. Kaspary
Instituto Nacional de Investigación Agropecuaria -INIA La
Estanzuela, Colonia, Uruguay
&
oleracea, Raphanus raphanistrum, Sida rhombifolia,
Solanum americanum, S. pseudocapsicum,
S. sisymbriifolium, Sonchus oleraceus and Talinum
paniculatum, representing 72.2% of the species
assessed. The species Conyza bonariensis, Cyperus
rotundus, Digitaria horizontalis, D. insularis,
Echinochloa colonum, Eleusine indica, Lolium
m u l t i f l o r u m , P o l y g o n u m h y d ro p i p e ro i d e s ,
Rhynchelytrum repens and Senecio brasiliensis were
resistant to M. ethiopica (RF < 1.0). Based on the new
host records presented, it is vital that control of weed
species within agricultural fields are considered as part
of effective management of M. ethiopica.
Keywords Invasive plants . Host status . Nematode
reproduction . Susceptibility . Root-knot nematodes
Vegetable production faces several issues, biotic factors
include insect pests, diseases and weeds, in addition to
abiotic factors such as drought, floods, and low soil
fertility (Nordey et al. 2017). Weeds are also important
biotic variables, which can limit crop yields. Weeds may
reduce crop yield by competing for resources, namely
nutrients, light, water, space, by allelopathic effects and
reducing food, feed, and fiber quality (Bridges 1994;
Sturm et al. 2018). In general, weeds produce large
amounts of seeds, which are capable of remaining viable
for long periods in the soil (Vivian et al. 2018). In
addition, weeds can act as alternative hosts of pests,
vectors and diseases (Bellé et al. 2017a).

Weed species facilitate reproduction of many plant-
parasitic nematodes and can therefore sustain nematode
populations during off season periods (Hillocks 1998).
A wide range of weeds associated with agricultural
crops are excellent hosts for root-knot nematode
(Meloidogyne spp.) species (Ramos et al. 2019). Con-
sequently, Meloidogyne species have been reported as
parasites of various species of weeds in different agri-
cultural areas worldwide (Castillo et al. 2008; Mônaco
et al. 2009; Bellé et al. 2017a), maintaining or increasing
population levels, and hindering control strategies.
Meloidogyne ethiopica Whitehead is considered to be
one of the most economically important nematode spe-
cies, due to being polyphagous and highly virulent. In
Brazil, M. ethiopica has been found associated with
numerous important agricultural crops, such as Solanum
lycopersicum L. (tomato), Glycine max (L.) Merrill (soy-
bean), Nicotiana tabacum L. (tobacco), Saccharum spp.
L. (sugarcane), Phaseolus vulgaris L. (common bean)
and Cucumis melo L. (melon) (Carneiro et al. 2008;
Castro et al. 2003; Gomes et al. 2005; Bellé et al.
2016b, c, 2017b). Thus, this species is able to parasitize
several economically important agricultural crops and
can be difficult to control (Strajnar and Širca 2011).
The capability of weed species to host
M. paranaenses Carneiro et al., M. incognita (Kofold
& White) Chitwood, and M. javanica (Treub) Chitwood
is well established (Mônaco et al. 2008; Silva et al.
2013; Balardin et al. 2019). However, with the excep-
tion of few reports on parasitism of M. ethiopica on
weeds in the field (Lima-Medina et al. 2013; Bellé
et al. 2016a), there are no controlled studies addressing
resistance and susceptibility of weeds to this nematode
species. Therefore, this study aimed to evaluate the
reaction of 36 weed species to a population of
M. ethiopica.
The experiment was conducted and replicated in two
independent trials from March to July 2018 to assess the
reaction of 36 different species of weeds (Table 1), to
evaluate the reproduction of a population of
M. ethiopica in greenhouse conditions, with temperature
of 25 ± 3 °C. A completely randomized experimental
design was used with six replications. The substrate
used in the experiment consisted of a mixture of sand
and soil (at a ratio of 2:1), which was disinfected by
autoclaving. The soil used in the experiment is classified
as Rhodic Ferralsol (clayic) (IUSS Working Group
WRB 2015), with the following physic chemical prop-
erties: clay = 48%; water pH value = 6.5; Shoemaker,
Eur J Plant Pathol
MacLean, and Pratt (SMP) test = 6.5; organic matter =
3.1%; P = 10.9 mg dm−3; K = 88 mg dm−3; Ca = 5.3
cmolc dm−3; Mg = 5.0 cmolc dm−3; and S = 9 cmolc
dm−3. Ten days after emergence, the seedlings were
transplanted to 2000-dm3 pots containing substrate,
one plant per pot.
The population of M. ethiopica used was identified
from the roots of Phaseolus vulgaris, collected in
Caiçara municipality, Northwest Rio Grande do Sul
State, Brazil (Bellé et al. 2016c), and was multiplied
on potted tomato plants (Solanum lycopersicum cv.
Santa Cruz). The inoculum of the nematode was obtain-
ed from the root system of plants kept at greenhouse
conditions (25 ± 3 °C), using the method of Hussey and
Barker (1973). The plants were inoculated five days
after transplanting with a suspension of 5000 eggs and
second-stage juvenile nematode (J2) specimens into
three inoculation holes of approximately two centime-
ters in depth, dug around the plant base. ‘Santa Cruz’
tomatoes were used as the viability control standard for
the inoculum.
Sixty days after inoculation, the root system of each
plant was washed individually under running water with
the excess water removed using paper towels before
being weighed. Nematode galls observed on the roots
were counted according the methodology proposed by
Taylor and Sasser (1978). After counting the number of
galls, the root systems were processed following the
method of Hussey and Barker (1973), to obtain the final
suspension of nematode population for quantification.
This number was used to obtain the reproduction factor
(final nematode population (Pf)/initial population (num-
ber of eggs plus J2 used in the nematode inoculations)
(Pi)), methodology proposed by Oostenbrink (1966),
where the weeds were classified as RF = 0 for immune,
RF < 1 for resistant and RF > 1 for susceptible. In addi-
tion, the number of nematodes per gram of root were
determined by the ratio between the total number of
nematodes and the total mass of the roots in grams
(Nema (g)) of each replicate.
The data for final nematode population and the re-
production variables were analyzed for normality by the
Shapiro-Wilk test, and for homoscedasticity by the
Hartley test. Subsequently, the data were subjected to
analysis of variance (p ≤ 0.05), and the treatments means
were compared by the Scott-Knott test at a probability
level of 5%, using the Genes software (Cruz 2006).
The data obtained for resistance (R) and susceptibil-
ity (S) for the different weeds in the first trial were
Eur J Plant Pathol

Table 1 Family, scientific name,

and common name of weed spe- Family Scientific name Common name
cies used in the present study
Amaranthaceae Amaranthus deflexus L. Large-fruit amaranth
Amaranthus hybridus L. Slim amaranth
Amaranthus spinosus L. Spiny amaranth
Amaranthus viridis L. Green amaranth
Asteraceae Acanthospermum australe (Loefl.) Kuntze Paraguay starburr
Bidens pilosa (L.) DC. Hairy beggarticks
Bidens subalternans DC. Beggar’s-ticks
Conyza bonariensis (L.) Cronquist Hairy fleabane
Galinsoga parviflora Cav. Gallant soldier
Senecio brasiliensis (Spreng.) Less. Flower-of-souls
Sonchus oleraceus L. Common sowthistle
Brassicaceae Raphanus raphanistrum L. Wild radish
Commelinaceae Commelina benghalensis L. Benghal dayflower
Convolvulaceae Ipomoea grandifolia (Dammer) O’Donell Morning glory
Ipomoea nil (L.) Roth. Morning glory
Ipomoea purpurea (L.) Roth. Morning glory
Cyperaceae Cyperus rotundus L. Nutgrass
Euphorbiaceae Euphorbia heterophylla L. Fireplant
Lamiaceae Leonurus sibiricus L. Honeyweed
Malvaceae Sida rhombifolia L. Arrowleaf sida
Oxalidaceae Oxalis corniculata L. Creeping woodsorrel
Poaceae Cynodon dactylon (L.) Pers. Bermuda grass
Digitaria horizontalis Willd. (Digho) Crabgrass; Sourgrass
Digitaria insularis (L.) Fedde Sourgrass
Echinochloa colonum (L.) Link Jungle rice
Eleusine indica (L.) Gaertn Indian goosegrass
Lolium multiflorum Lam. Ryegrass
Rhynchelytrum repens (Willd.) C.E.Hubb Natal grass
Polygonaceae Polygonum hydropiperoides (Michx.) Small Swamp smartweed
Portulacaceae Portulaca oleracea L. Verdolaga; Red root
Sapindaceae Cardiospermum halicacabum L. Balloon vine
Solanaceae Nicandra physaloides (L.) Gaertn. Apple-of-Peru
Solanum americanum Mill. American black nightshade
Solanum pseudocapsicum L. Jerusalem cherry
Solanum sisymbriifolium Lam. Sticky nightshade
Talinaceae Talinum paniculatum (Jacq.) Gaertn Fameflower

confirmed in the second trial, indicating reproducibility
and assurance of the obtained results (Table 2). The
different species of weeds exhibited a significant (p ≤
0.05) to the parasitism and susceptibility to
M. ethiopica, based on the gall index (GI), number of
nematodes per gram of root (Nema/g) and reproduction
factor (RF), compared to the control. The viability of the
nematode inoculum was confirmed by the reproduction
factor found (RF >24,5) for the control ‘Santa Cruz’
tomato plants (Table 2).
According to the obtained data, 72.2% of the weed
species evaluated were susceptible to M. ethiopica
(RF ≥ 1.0) (Table 2). The weed species considered sus-
ceptible to M. ethiopica: Acanthospermum australe,
 Eur J Plant Pathol

Table 2 Host status of weeds to Meloidogyne ethiopica under controlled conditions two months after nematode inoculation carried out in
2018

SPECIES Trial 1 Trial 2

FRW (g)1 GI 2 Nema (g) 3 RF 4 Reaction FRW (g) GI Nema (g) RF Reaction

Acanthospermum australe 8.8 2.5 C6 743 E 1.3 D S 15.0 3.0 C 700 D 2.1 D S
Amaranthus deflexus 15.1 4.5 A 1993 C 6.0 C S 20.5 4.0 B 1341 C 5.5 C S
Amaranthus hybridus 15.8 4.5 A 1628 C 5.1 C S 21.5 4.5 A 1047 C 4.5 C S
Amaranthus spinosus 16.8 5.0 A 1956 C 6.6 C S 22.5 4.5 A 1667 C 7.5 C S
Amaranthus viridis 13.7 3.5 B 1648 C 4.5 C S 20.0 4.0 B 900 C 3.6 C S
Bidens pilosa 4.2 1.5 C 3452 B 2.9 D S 19.9 4.0 B 575 D 2.3 D S
Bidens subalternans 3.5 1.0 D 3000 B 2.1 D S 17.5 3.5 B 543 D 1.9 D S
Cardiospermum halicacabum 5.6 1.5 C 3571 B 4.0 C S 17.3 3.5 B 1000 C 3.5 C S
Commelina benghalensis 14.4 4.5 A 871 E 2.5 D S 25.0 5.0 A 1340 C 6.7 C S
Conyza bonariensis 3.3 1.0 D 714 E 0.5 E R 5.0 1.0 D 300 D 0.3 E R
Cynodon dactylon 7.4 2.0 C 1156 D 1.7 D S 7.5 1.5 C 800 C 1.2 D S
Cyperus rotundus 4.2 1.5 C 893 E 0.8 E R 5.0 1.0 D 550 D 0.5 E R
Digitaria horizontalis 3.5 1.0 D 571 E 0.4 E R 4.0 1.0 D 250 D 0.2 E R
Digitaria insularis 3.4 1.0 D 429 E 0.3 E R 4.7 1.0 D 430 D 0.4 E R
Echinochloa colonum 3.6 1.0 D 1143 D 0.8 E R 5.0 1.0 D 700 D 0.7 E R
Eleusine indica 4.2 1.5 C 655 E 0.6 E R 5.0 1.0 D 500 D 0.5 E R
Euphorbia heterophylla 12.3 3.5 B 612 E 1.5 D S 12.5 2.5 C 520 D 1.3 D S
Galinsoga parviflora 14.7 4.5 A 2041 C 6.0 C S 24.6 5.0 A 1020 C 5.1 C S
Ipomoea grandifolia 12.3 3.5 B 2122 C 5.2 C S 22.5 4.5 A 1022 C 4.6 C S
Ipomoea nil 14.0 4.0 B 2250 C 6.3 C S 20.0 4.0 B 1275 C 5.1 C S
Ipomoea purpurea 12.3 3.5 B 2367 C 5.8 C S 19.7 4.0 B 1100 C 4.4 C S
Leonurus sibiricus 17.5 5.0 A 1143 D 4.0 C S 17.5 3.5 B 1057 C 3.7 C S
Lolium multiflorum 3.5 1.0 D 429 E 0.3 E R 5.0 1.0 D 200 D 0.2 E R
Nicandra physaloides 16.5 5.0 A 1600 C 5.6 C S 17.5 3.5 B 943 C 3.3 C S
Oxalis corniculata 17.1 5.0 A 4543 A 15.9 A S 25.0 5.0 A 3700 A 18.5 A S
Polygonum hydropiperoides 5.3 1.5 C 571 E 0.6 E R 5.0 1.0 D 200 D 0.2 E R
Portulaca oleracea 17.8 5.0 A 3514 B 12.3 B S 25.1 5.0 A 2840 B 14.2 B S
Raphanus raphanistrum 8.8 2.5 C 2000 C 3.5 C S 10.0 2.0 C 1400 C 2.8 C S
Rhynchelytrum repens 3.5 1.0 D 643 E 0.5 E R 5.0 1.0 D 600 D 0.6 E R
Senecio brasiliensis 6.3 2.0 C 635 E 0.8 E R 7.5 1.5 C 393 D 0.59 E R
Sida rhombifolia 14.5 5.0 A 5743 A 20.1 A S 16.2 5.0 A 4700 A 15.2 B S
Solanum americanum 17.1 5.0 A 6143 A 21.5 A S 30.0 5.0 A 4300 A 25.8 A S
Solanum pseudocapsicum 16.9 5.0 A 5286 A 18.5 A S 28.9 5.0 A 4060 A 23.5 A S
Solanum sisymbriifolium 17.2 5.0 A 5600 A 19.6 A S 86.7 5.0 A 1240 C 21.5 A S
Sonchus oleraceus 4.2 1.5 C 5000 A 4.2 C S 33.4 2.5 C 3040 B 20.3 A S
Talinum paniculatum 17.5 5.0 A 3514 B 12.3 B S 3.0 5.0 A 5160 A 3.1 C S
Solanum lycopersicum 17.0 5.0 9286 32.5 – 25.0 5.0 8040 40.2 –
CV (%) – 20.3 25.8 24.5 – – 19.5 22.0 26.3 –
1
Fresh root weight
2
Galls Index based on Taylor and Sasser (1978): 0 = no galls; 1 = 1–2; 2 = 3–10; 3 = 11–30; 4 = 31–100 and 5 = more than 100 galls per root
system
3
Number of nematodes per gram of root: ratio between total nematodes and total root mass
4
RF = Final population/Initial population
5
Reaction based on Oostenbrink (1966): resistant (R) (RF < 1.0) and susceptible (S) (RF ≥ 1.0)
6
Means followed by the same letter in each column do not differ significantly by the Scott-Knott test at 5% probability
Eur J Plant Pathol
Amaranthus deflexus, Amaranthus hybridus,
Amaranthus spinosus, Amaranthus viridis, Bidens
pilosa, Bidens subalternans, Cardiospermum
halicacabum, Commelina benghalensis, Cynodon
dactylon, Euphorbia heterophylla, Galinsoga
parviflora, Ipomoea grandifolia, Ipomoea nil, Ipomoea
purpurea, Leonurus sibiricus, Nicandra physaloides,
Oxalis corniculata, Portulaca oleracea, Raphanus
raphanistrum, Sida rhombifolia, Solanum americanum,
Solanum pseudocapsicum, Solanum sisymbriifolium,
Sonchus oleraceus and Talinum paniculatum (Table 2).
In addition, the following weed species, O. corniculata,
P. oleracea, R. raphanistrum, S. rhombifolia S.
americanum, S, pseudocapsicum, S. sisymbriifolium
and T. paniculatum (Table 2), presented high gall index
and nematodes per gram of root, with mean values of GI
equal to the control (5 for S. esculentum). While the
highest average amount of nematodes per gram of root
was obtained in S. rombifolia and S. americanum
(Nema/g > 5200).
Among susceptible species, O. corniculata, S.
americanum, S. sisymbriifolium and S. pseudocapsicum
presented the highest reproduction factors (RF) with
mean values for the two experiments 17.2, 23.6, 20.5
and 21.0, respectively (Table 2). Therefore, these spe-
cies can be considered excellent hosts of M. ethiopica,
with potential to increase the population of this nema-
tode even in the absence of agricultural crops. These
species of weeds can also act as hosts for other
phytonematodes of the genus Meloidogyne;
O. corniculata is susceptible to M. javanica and
M. paranaensis (Mônaco et al. 2009); S. americanum
is susceptible to M. incognita and M. javanica (Silva
et al. 2013) and S. sisymbriifolium and
S. pseudocapsicum are susceptible to M. enterolobii
(Bellé et al. 2019). As a consequence, the presence of
these weed species in cropping areas may negatively
impact on yields by sustaining or even increasing nem-
atode population levels in the absence of a host crop.
Other weed species evaluated in the study (27.8%)
were deemed to be resistant (RF <1.0), with no immune
species observed (RF = 0). Therefore, M. ethiopica re-
sistant species were: Conyza bonariensis, Cyperus
rotundus, Digitaria horizontalis, Digitaria insularis,
Echinochloa colonum, Eleusine indica, Lolium
m u l t i f l o r u m , P o l y g o n u m h y d ro p i p e ro i d e s ,
Rhynchelytrum repens and Senecio brasiliensis
(Table 2). However, other studies reported the suscepti-
bility of these weeds to other Meloidogyne nematodes,
for example the species E. colonum as susceptible to
M. incognita and M. javanica (Silva et al. 2013). In
another study evaluating the reaction of different weeds
to M. enterolobii, the species C. bonariensis,
C. rotundus, D. horizontalis, D. insularis, E. indica e
S. brasiliensis were resistant, whereas
P. hydropiperoides and R. repens were considered sus-
ceptible (Bellé et al. 2019).
Meloidogyne ethiopica is considered to be an eco-
nomically important emerging pest species, being
placed on the alert list of the European and Mediterra-
nean Plant Protection Organization (EPPO) in 2011. In
South America, this nematode is associated with the
decline of grapevine in Chile (Carneiro et al. 2007),
and was also found parasitizing commercial asparagus
(Asparagus officinalis L.) plantations in Peru (Murga-
Gutierrez et al. 2012). In Brazil, the first record of
M. ethiopica was parasitizing the roots of Actinidia
deliciosa Chevalter (Carneiro et al. 2003), and later in
soybean (Glycine max) (Castro et al. 2003), which is
currentlythe most important economic crop in the coun-
try. Recently, this nematode was reported parasitizing
several crops of economic importance in Brazil, such as
Polymnia sonchifolia Poepp (yacon) and Solanum
esculentum (Carneiro et al. 2008); Saccharum spp. (sug-
arcane), Phaseolus vulgaris (common bean) and
Cucumis melo (melon) (Bellé et al. 2016b, 2017b).
In addition, M. ethiopia was recently detected para-
sitizing Sida rhombifolia (Lima-Medina et al. 2013) and
Oxalis corniculata (Bellé et al. 2016a) which are com-
mon weed species in several cultivated areas of Brazil,
indicating that this nematode is likely widely distributed
across agricultural areas. Although there are limited
reports on its distribution and pathogenicity, where re-
corded this species has caused significant damage to
host plants (Lima-Medina et al. 2014). To compound
this issue, certain weed hosts of M. ethiopica are resis-
tant to herbicides. An aggravating issue in the presence
of host plants of M. ethiopica that are resistant to herbi-
cides. In Brazil, due to the predominance of glyphosate-
resistant row crops, an increase in selection pressure of
resistant biotypes to this herbicide has occurred (Silva
et al. 2017a). Farmers in the country have observed the
occurrence of biotypes of Conyza spp. resistant to
glyphosate, Clhorimurin, 2,4-d, paraquat, diuron and
salflufenacil; Digitaria insularis and Eleusine indica
resistant to glyphosate and herbicides inhibitors of
ACCase, and Bidens pilosa with herbicide resistance
inhibitor of FSII and ALS-Inhibiting (Silva et al.

2017b; Heap 2019). The presence of these weeds in
cultivated areas facilitates the maintenance and increase
of M. ethiopica populations.
This study identified new host records for
M. ethiopica, frequently found in agricultural areas, by
a direct evaluation of host and efficiency of reproduc-
tion. Understanding the ability of M. ethiopica to para-
sitize a wide range of weed plant species, and thus
survive and increase its population numbers in the ab-
sence of an agricultural host crop, is vital for effective
management practices and control of nematode popula-
tions in agricultural land.
Compliance with ethical standards
Conflict of interest The authors declare that they have no con-
flict of interest.
Research involving human participants and/or animals This
article does not contain any studies with human participants or
animals performed by any of the authors.
Informed consent Informed consent was obtained from all in-
dividual participants included in the study.
References
Balardin, R. R., Bellé, C., Ramos, R. F., Sobucki, L., Nora, D. D.,
Antoniolli, Z. I. (2019). Reação de plantas daninhas a
Meloidogyne javanica. Ciências Agrárias: Campo
Promissor em Pesquisa 5. 5ed.: Atena Editora, 149-157.
https://doi.org/10.22533/at.ed.19119200617.
Bellé, C., Kaspary, T. E., Schmitt, J., & Kuhn, P. R. (2016a).
Meloidogyne ethiopica and Meloidogyne arenaria parasitiz-
ing Oxalis corniculata in Brazil. Autralasian Plant Disease
Notes, 11, 24.
Bellé, C., Kulczynski, S. M., Kuhn, P. R., Carneiro, R. M. D. G.,
Lima-Medina, I., & Gomes, C. B. (2016b). First report of
Meloidogyne ethiopica parasitizing sugarcane in Brazil.
Plant Disease, 102, 1204–1205.
Bellé, C., Kuhn, P. R., Kaspary, T. E., Groth, M. Z., Schmitt, J., &
Kulczynski, S. M. (2016c). Parasitization of the common
bean (Phaseolus vulgaris) by Meloidogyne ethiopica in
southern Brazil. Plant Disease, 101(3), 510.
Bellé, C., Kulczynski, S. M., Kaspary, T. E., & Kuhn, P. R.
(2017a). Plantas daninhas como hospedeiras alternativas para
Meloidogyne incognita. Nematropica, 47, 26–33.
Bellé, C., Kaspary, T. E., Groth, M. Z. G., & Cocco, K. L. T.
(2017b). Meloidogyne ethiopica parasitizing melon fields in
Rio Grande do Sul state, Brazil. Journal of Plant Diseases
and Protection, 124(4), 393–397.
Eur J Plant Pathol
Bellé, C., Ramos, R. F., Ballardin, R. R., Kaspary, T. E., &
Antoniolli, Z. I. (2019). Reproduction of Meloidogyne
enterolobii on different weeds. Tropical Plant Pathology,
44, 380–384. https://doi.org/10.1007/s40858-019-00278-z.
Bridges, D. C. (1994). Impact of weeds on human endeavors.
Weed Technology, 8, 392–395.
Carneiro, R. M. D. G., Gomes, C. B., Almeida, M. R., Gomes, A.
C. C., & Martins, I. (2003). Primeiro registro de Meloidogyne
ethiopica em plantas quivi no Brasil e reação em diferentes
plantas hospedeiras. Nematologia Brasileira, 27(2), 152–
158.
Carneiro, R. M. D. G., Almeida, M. R. A., Cofcewicz, E. T.,
Magunacelaya, J. C., & Aballay, E. (2007). Meloidogyne
ethiopica, a major root-knot nematode parasitising Vitis vi-
nifera and other crops in Chile. Nematology, 9(5), 635–641.
Carneiro, R. M. D. G., Almeida, M. R. A., Martins, I., Souza, J. F.,
Pires, A. Q., & Tigano, M. S. (2008). Ocorrência de
Meloidogyne spp. e fungos nematófagos em hortaliças no
Distrito Federal, Brasil. Nematologia Brasileira, 32(2), 135–
141.
Castillo, P., Rapoport, H. F., Rius, J. E. P., & Díaz, R. M. J. (2008).
Suitability of weed species prevailing in Spanish vineyards as
hosts for root-knot nematodes. European Journal of Plant
Pathology, 120, 43–51. https://doi.org/10.1007/s10658-007-
9195-8.
Castro, J. M. C., Lima, R., & Carneiro, R. M. D. C. (2003).
Variabilidade isoenzimática de populações de Meloidogyne
spp. proveniente de regiões brasileiras produtoras de soja.
Nematologia Brasileira, 27, 1–12.
Cruz, C. D. (2006). Programa Genes – Estatística Experimental e
Matrizes. Viçosa: Editora UFV.
Gomes, C. B., Carbonari, J. J., Medina, I. L., & Lima, D. L.
(2005). Levantamento de Meloidogyne ethiopica em viveiros
de quivi no Rio Grande do Sul e registro de sua ocorrência
em Nicotiana tabacum e Sida rhombifolia. Nematologia
Brasileira, 29, 114.
Heap, I. (2019) The international survey of herbicide resistant
weeds. http://www.weedscience.com. Accessed Fev 12,
2019.
Hillocks, R. J. (1998). The potential benefits of weeds with refer-
ence to small holder agriculture in Africa. Integrated Pest
Management Reviews, 3, 155–167.
Hussey, R. S., & Barker, K. R. (1973). A comparison of methods
of collecting inocula of Meloidogyne spp., including a new
technique. Plant Disease Reporter, 57, 1025–1028.
IUSS WORKING GROUP, W. R. B. et al. (2015) World reference
base for soil resources. World Soil Resources Report, v. 103.
Lima-Medina, I., Somavilla, L., Carneiro, R. M. D. G., & Gomes,
C. B. (2013). Espécies de Meloidogyne em figueira (Ficus
carica) e em plantas infestantes. Nematropica, 43(1), 56–62.
Lima-Medina, I., Coila, V. H. C., Gomes, C. B., Pereira, A. S., &
Nazareno, N. R. X. (2014). Ocorrência de M. ethiopica no
Paraná e reação de cultivares de batata ao nematoide das
galhas. Horticultura Brasileira, 32(4), 482–485.
Mônaco, A. P. A., Carneiro, R. G., Kranz, W. M., Gomes, J. C.,
Scherer, A., Nakamura, K. C., et al. (2008). Reação de
espécies de plantas daninhas a Meloidogyne paranaenses.
Nematologia Brasileira, 32, 279–284.
Mônaco, A. P. A., Carneiro, R. G., Kranz, W. M., Gomes, J. C.,
Scherer, A., & Santiago, D. C. (2009). Reação de espécies de
plantas daninhas a Meloidogyne incognita Raças 1 e 3, a
Eur J Plant Pathol
M. javanica e a M. paranaenses. Nematologia Brasileira,
33(3), 235–242.
Murga-Gutierrez, S. N., Colagiero, M., Rosso, L. C., Sialer, M. M.
F., & Ciancio, A. (2012). Root-knot nematodes from aspar-
agus and associated biological antagonists in Peru.
Nematropica, 42, 57–62.
Nordey, T., Basset-Mens, C., Bon, H. D., Martin, T., Déletre, E.,
Simon, S., et al. (2017). Protected cultivation of vegetable
crops in sub-Saharan Africa: Limits and prospects for small-
holders. A review. Agronomy for Sustainable Development,
37, 53.
Oostenbrink, M. (1966). Major characteristic of relation between
nematodes and plants. Mededelingen Landbouwhogeschool,
66(1), 1–46.
Ramos, R. F, Kaspary, T. E., Balardin, R. R., Dalla Nora, D.,
Antoniolli, Z. I., & Bellé, C. (2019) Plantas daninhas como
hospedeiras dos nematoides-das-galhas. Revista Agronomia
Brasileira, 3, rab201906. https://doi.org/10.29372/rab201906
Silva, S. L. S., Santos, T. F. S., Ribeiro, N. R., Silvério, A. T., &
Morais, T. S. (2013). Reação de plantas daninhas a
Meloidogyne incognita e M. javanica. Nematologia
Brasileira, 37, 57–60.
Silva, A. F., Karam, D., Gazziero, D. L. P., Adegas, F. S., Vargas,
L., & Silva, W. T. (2017a). Monitoramento de resistência de
plantas daninhas a herbicidas no Estado de Mato Grosso –
Safra 2016/2017. Circular Técnica, 228, 1–5.
Silva, A. F., Karam, D., Silva, W. T., Vargas, L., Gazziero, D. L. P.,
& Adegas, F. S. (2017b). Percepção da ocorrência de plantas
daninhas resistentes a herbicidas por produtores de soja -
milho safrinha no Estado de Mato Grosso. Documentos
Embrapa Milho e Sorgo, 209, 1–28.
Strajnar, P., & Širca, S. (2011). The effect of some insecticides,
natural compounds and tomato cv. Venezia with mi gene on
the nematode Meloidogyne ethiopica (Nematoda) reproduc-
tion. Acta Agriculturae Slovenica, 97, 5–10.
Sturm, D. J., Peteinatos, G., & Gerhards, R. (2018). Contribution
of allelopathic effects to the overallweed suppression by
different cover crops. Weed Research, 58, 331–337.
Taylor, A. L., & Sasser, J. N. (1978). Biology, identification and
control of root-knot nematodes. North Carolina State
University, Raleigh: Department of Plant Pathology.
Vivian, R., Silva, A. A., Gimenes Jr., M., Fagan, E. B., Ruiz, S. T.,
& Labonia, V. (2018). Dormência em sementes de plantas
daninhas como mecanismo de sobrevivência – Breve revisão.
Planta Daninha, 26, 695–706.